Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamics

15 p.-8 fig.

Detalles Bibliográficos
Autores: Mónico, Andreia, Duarte, Sofia, Pajares, María Ángeles, Pérez-Sala, Dolores
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/175623
Acceso en línea:http://hdl.handle.net/10261/175623
Access Level:acceso abierto
Palabra clave:Vimentin
Lipoxidation
HNE
Cyclopentenone prostaglandins
Intermediate filaments
Vimentin filament morphology and dynamics
Vimentin oxidation
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spelling Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamicsMónico, AndreiaDuarte, SofiaPajares, María ÁngelesPérez-Sala, DoloresVimentinLipoxidationHNECyclopentenone prostaglandinsIntermediate filamentsVimentin filament morphology and dynamicsVimentin oxidation15 p.-8 fig.The intermediate filament protein vimentin constitutes a critical sensor for electrophilic and oxidative stress, which induce extensive reorganization of the vimentin cytoskeletal network. Here, we have investigated the mechanisms underlying these effects. In vitro, electrophilic lipids, including 15-deoxy-Δ12,14-prostaglandin J2 (15d-PGJ2) and 4-hydroxynonenal (HNE), directly bind to vimentin, whereas the oxidant diamide induces disulfide bond formation. Mutation of the single vimentin cysteine residue (Cys328) blunts disulfide formation and reduces lipoxidation by 15d-PGJ2, but not HNE. Preincubation with these agents differentially hinders NaClinduced filament formation by wild-type vimentin, with effects ranging from delayed elongation and increased filament diameter to severe impairment of assembly or aggregation. Conversely, the morphology of vimentin Cys328Ser filaments is mildly or not affected. Interestingly, preformed vimentin filaments are more resistant to electrophile-induced disruption, although chemical modification is not diminished, showing that vimentin (lip) oxidation prior to assembly is more deleterious. In cells, electrophiles, particularly diamide, induce a fast and drastic disruption of existing filaments, which requires the presence of Cys328. As the cellular vimentin network is under continuous remodeling, we hypothesized that vimentin exchange on filaments would be necessary for diamide-induced disruption. We confirmed that strategies reducing vimentin dynamics, as monitored by FRAP, including cysteine crosslinking and ATP synthesis inhibition, prevent diamide effect. In turn, phosphorylation may promote vimentin disassembly. Indeed, treatment with the phosphatase inhibitor calyculin A to prevent dephosphorylation intensifies electrophile-induced wild-type vimentin filament disruption. However, whereas a phosphorylation-deficient vimentin mutant is only partially protected from disorganization, Cys328Ser vimentin is virtually resistant, even in the presence of calyculin A. Together, these results indicate that modification of Cys328 and vimentin exchange are critical for electrophile-induced network disruption.This work was supported by the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie Grant agreement no. 675132 “Masstrplan”, Grant SAF2015-68590-R from MINECO/FEDER, Spain and Instituto de Salud Carlos III/FEDER,RETIC Aradyal RD16/0006/0021. Feedback from COST Action CA15214 “EuroCellNet” is gratefully acknowledged.Peer reviewedElsevierEuropean CommissionMinisterio de Economía y Competitividad (España)Instituto de Salud Carlos IIIMónico, Andreia [0000-0003-4855-8241]Pajares, María A. [0000-0002-4714-9051]Pérez-Sala, Dolores [0000-0003-0600-665X]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]201920192019info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/175623reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/EC/H2020/675132info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2015-68590-Rhttps://doi.org/10.1016/j.redox.2019.101098Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/1756232026-05-22T06:33:51Z
dc.title.none.fl_str_mv Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamics
title Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamics
spellingShingle Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamics
Mónico, Andreia
Vimentin
Lipoxidation
HNE
Cyclopentenone prostaglandins
Intermediate filaments
Vimentin filament morphology and dynamics
Vimentin oxidation
title_short Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamics
title_full Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamics
title_fullStr Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamics
title_full_unstemmed Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamics
title_sort Vimentin disruption by lipoxidation and electrophiles: Role of the cysteine residue and filament dynamics
dc.creator.none.fl_str_mv Mónico, Andreia
Duarte, Sofia
Pajares, María Ángeles
Pérez-Sala, Dolores
author Mónico, Andreia
author_facet Mónico, Andreia
Duarte, Sofia
Pajares, María Ángeles
Pérez-Sala, Dolores
author_role author
author2 Duarte, Sofia
Pajares, María Ángeles
Pérez-Sala, Dolores
author2_role author
author
author
dc.contributor.none.fl_str_mv European Commission
Ministerio de Economía y Competitividad (España)
Instituto de Salud Carlos III
Mónico, Andreia [0000-0003-4855-8241]
Pajares, María A. [0000-0002-4714-9051]
Pérez-Sala, Dolores [0000-0003-0600-665X]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Vimentin
Lipoxidation
HNE
Cyclopentenone prostaglandins
Intermediate filaments
Vimentin filament morphology and dynamics
Vimentin oxidation
topic Vimentin
Lipoxidation
HNE
Cyclopentenone prostaglandins
Intermediate filaments
Vimentin filament morphology and dynamics
Vimentin oxidation
description 15 p.-8 fig.
publishDate 2019
dc.date.none.fl_str_mv 2019
2019
2019
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/175623
url http://hdl.handle.net/10261/175623
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/EC/H2020/675132
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2015-68590-R
https://doi.org/10.1016/j.redox.2019.101098
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.812429

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